Spermin Anatomisi, Erkek Genital Organındaki Yolculuğu ve Kapasitasyon
Özet
Memeli spermatozoonları, yalnızca döllenme amacıyla evrimleşmiş, yüksek derecede özelleşmiş ve bölümlenmiş hücrelerdir. Sperm başı, protaminlerle paketlenmiş hiper yoğunlaşmış DNA, indirgenmiş bir nükleer zarf ve zona pellucida’yı aşmayı sağlayan enzimleri içeren akrozomu barındırır. Kuyruk, orta parça, ana parça ve son parçadan oluşur ve hareketliliğini aksonemin korunan 9+2 mikrotübül düzeni ile sağlar. Dış ve iç dinein kolları, dinein düzenleyici kompleksi ve post-translasyonel modifikasyonlar tarafından düzenlenerek mikrotübül kaymasını koordine eder ve flagellar dalgaların oluşumunu sağlar. Kalsiyum iyonları (Ca²⁺), eğrilik, vuruş simetrisi ve hareketliliğin kritik düzenleyicisidir; orta parçadaki mitokondrilerin Ca²⁺ homeostazına katkısı olabileceği düşünülmektedir. Ejakülasyon sonrasında, spermatozoonlar kapasitasyon olarak bilinen ve fizyolojik, biyokimyasal ve moleküler değişiklikleri içeren bir süreçten geçmeden döllenme yeteneği kazanamaz. Kapasitasyon hızlı ve yavaş olaylar olarak iki faza ayrılır. Hızlı olaylar, Na⁺/HCO₃⁻ kotransportörü aracılığıyla bikarbonat girişini, çözünebilir adenilat siklazın (sAC) aktivasyonunu, siklik AMP (cAMP) ve protein kinaz A (PKA) aktivitesindeki artışı, iyon kanalı modülasyonunu (ör. CatSper), fosfolipid karışmasını ve kolesterol yeniden dağılımını içerir. Yavaş olaylar ise albümin gibi kolesterol alıcılarını, sürdürülen cAMP düzeylerini ve başlıca Src ailesi kinazlar tarafından gerçekleştirilen protein tirozin fosforilasyonunu gerektirir; fare ve insan spermlerinde bu kinazların rolleri farklılık gösterir. Ca²⁺, kapasitasyonun her iki fazını da etkiler ve bağlama bağlı olarak uyarıcı veya baskılayıcı etki gösterebilir. Özellikle farelerde yapılan deneyler, hücre içi Ca²⁺ seviyelerinin yapay olarak yükseltilmesinin cAMP/PKA’ya bağımlı yolları atlayarak “kapasitasyonu gerçekleşmemiş” spermatozoonların in vitro ortamda oositleri dölleyebilmesini sağladığını göstermektedir. Tüm bu bulgular, sperm yapısının özel tasarımını ve kapasitasyonun sıkı biçimde düzenlenen sinyal yollarını ortaya koymakta; Ca²⁺’ın döllenme biyolojisinde merkezi bir ikincil haberci olduğunu vurgulamaktadır.
Referanslar
Barratt, C.L., Kay, V., and Oxenham, S.K. (2009). The human spermatozoon - a stripped down but refined machine. J Biol. 8(7): p. 63.
Brewer, L., Corzett, M., and Balhorn, R. (2002). Condensation of DNA by Spermatid Basic Nuclear Proteins*. Journal of Biological Chemistry. 277(41): p. 38895-38900.
Dadoune, J.P. (2003). Expression of mammalian spermatozoal nucleoproteins. Microsc Res Tech. 61(1): p. 56-75.
Fauci, L.J. and Dillon, R. (2006). BIOFLUIDMECHANICS OF REPRODUCTION. Annual Review of Fluid Mechanics. 38(Volume 38, 2006): p. 371-394.
Oko, R.J. (1995). Developmental expression and possible role of perinuclear theca proteins in mammalian spermatozoa. Reprod Fertil Dev. 7(4): p. 777-97.
Bozkurt, H.H. and Woolley, D.M. (1993). Morphology of nexin links in relation to interdoublet sliding in the sperm flagellum. Cell Motil Cytoskeleton. 24(2): p. 109-18.
Brokaw, C.J. (2009). Thinking about flagellar oscillation. Cell Motility. 66(8): p. 425-436.
DiBella, L.M. and King, S.M. (2001). Dynein motors of the Chlamydomonas flagellum. Int Rev Cytol. 210: p. 227-68.
Porter, M.E. and Sale, W.S. (2000). The 9 + 2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J Cell Biol. 151(5): p. F37-42.
Takada, S., Wilkerson, C.G., Wakabayashi, K., Kamiya, R., and Witman, G.B. (2002). The outer dynein arm-docking complex: composition and characterization of a subunit (oda1) necessary for outer arm assembly. Mol Biol Cell. 13(3): p. 1015-29.
Brokaw, C.J. and Kamiya, R. (1987). Bending patterns of Chlamydomonas flagella: IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function. Cell Motility. 8(1): p. 68-75.
Brokaw, C.J., Josslin, R., and Bobrow, L. (1974). Calcium ion regulation of flagellar beat symmetry in reactivated sea urchin spermatozoa. Biochem Biophys Res Commun. 58(3): p. 795-800.
Inaba, K. (2002). Dephosphorylation of Tctex2-related dynein light chain by type 2A protein phosphatase. Biochem Biophys Res Commun. 297(4): p. 800-5.
Gagnon, C., White, D., Cosson, J., Huitorel, P., Eddé, B., Desbruyères, E., Paturle-Lafanechère, L., Multigner, L., Job, D., and Cibert, C. (1996). The polyglutamylated lateral chain of alpha-tubulin plays a key role in flagellar motility. J Cell Sci. 109 ( Pt 6): p. 1545-53.
Huitorel, P., White, D., Fouquet, J.P., Kann, M.L., Cosson, J., and Gagnon, C. (2002). Differential distribution of glutamylated tubulin isoforms along the sea urchin sperm axoneme. Mol Reprod Dev. 62(1): p. 139-48.
Lindemann, C.B. and Lesich, K.A. (2010). Flagellar and ciliary beating: the proven and the possible. J Cell Sci. 123(Pt 4): p. 519-28.
O'Rand, M.G. and Widgren, E.E. (2012). Loss of calcium in human spermatozoa via EPPIN, the semenogelin receptor. Biol Reprod. 86(2): p. 55.
Wennemuth, G., Babcock, D.F., and Hille, B. (2003). Calcium clearance mechanisms of mouse sperm. J Gen Physiol. 122(1): p. 115-28.
Harper, C., Wootton, L., Michelangeli, F., Lefièvre, L., Barratt, C., and Publicover, S. (2005). Secretory pathway Ca2+-ATPase (SPCA1) Ca2+ pumps, not SERCAs, regulate complex [Ca2+]i signals in human spermatozoa. Journal of Cell Science. 118(8): p. 1673-1685.
Chang, M.C. (1951). Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature. 168(4277): p. 697-8.
Austin, C.R. (1951). Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res B. 4(4): p. 581-96.
Aitken, R.J. and Nixon, B. (2013). Sperm capacitation: a distant landscape glimpsed but unexplored. Mol Hum Reprod. 19(12): p. 785-93.
Aitken, R.J., Harkiss, D., Knox, W., Paterson, M., and Irvine, D.S. (1998). A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation. J Cell Sci. 111 ( Pt 5): p. 645-56.
Aitken, R.J., Harkiss, D., Knox, W., Paterson, M., and Irvine, S. (1998). On the cellular mechanisms by which the bicarbonate ion mediates the extragenomic action of progesterone on human spermatozoa. Biol Reprod. 58(1): p. 186-96.
Baker, M.A., Hetherington, L., and Aitken, R.J. (2006). Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa. J Cell Sci. 119(Pt 15): p. 3182-92.
Ecroyd, H., Asquith, K.L., Jones, R.C., and Aitken, R.J. (2004). The development of signal transduction pathways during epididymal maturation is calcium dependent. Dev Biol. 268(1): p. 53-63.
Visconti, P.E., Bailey, J.L., Moore, G.D., Pan, D., Olds-Clarke, P., and Kopf, G.S. (1995). Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development. 121(4): p. 1129-37.
Devi, K.U., Jha, K., and Shivaji, S. (1999). Plasma membrane-associated protein tyrosine phosphatase activity in hamster spermatozoa. Mol Reprod Dev. 53(1): p. 42-50.
Galantino-Homer, H.L., Visconti, P.E., and Kopf, G.S. (1997). Regulation of Protein Tyrosine Phosphorylation during Bovine Sperm Capacitation by a Cyclic Adenosine 3',5'-Monophosphate-Dependent Pathway1. Biology of Reproduction. 56(3): p. 707-719.
Kalab, P., Peknicová, J., Geussová, G., and Moos, J. (1998). Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway. Mol Reprod Dev. 51(3): p. 304-14.
Luconi, M., Krausz, C., Forti, G., and Baldi, E. (1996). Extracellular calcium negatively modulates tyrosine phosphorylation and tyrosine kinase activity during capacitation of human spermatozoa. Biol Reprod. 55(1): p. 207-16.
Demarco, I.A., Espinosa, F., Edwards, J., Sosnik, J., De La Vega-Beltran, J.L., Hockensmith, J.W., Kopf, G.S., Darszon, A., and Visconti, P.E. (2003). Involvement of a Na+/HCO-3 cotransporter in mouse sperm capacitation. J Biol Chem. 278(9): p. 7001-9.
Chen, Y., Cann, M.J., Litvin, T.N., Iourgenko, V., Sinclair, M.L., Levin, L.R., and Buck, J. (2000). Soluble Adenylyl Cyclase as an Evolutionarily Conserved Bicarbonate Sensor. Science. 289(5479): p. 625-628.
Harrison, R.A., Ashworth, P.J., and Miller, N.G. (1996). Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev. 45(3): p. 378-91.
Gadella, B.M. and Harrison, R.A. (2002). Capacitation induces cyclic adenosine 3',5'-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod. 67(1): p. 340-50.
Flesch, F.M., Brouwers, J.F., Nievelstein, P.F., Verkleij, A.J., van Golde, L.M., Colenbrander, B., and Gadella, B.M. (2001). Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci. 114(Pt 19): p. 3543-55.
Boatman, D.E. and Robbins, R.S. (1991). Bicarbonate: carbon-dioxide regulation of sperm capacitation, hyperactivated motility, and acrosome reactions. Biol Reprod. 44(5): p. 806-13.
Gadella, B.M., Miller, N.G., Colenbrander, B., van Golde, L.M., and Harrison, R.A. (1999). Flow cytometric detection of transbilayer movement of fluorescent phospholipid analogues across the boar sperm plasma membrane: elimination of labeling artifacts. Mol Reprod Dev. 53(1): p. 108-25.
Lee, M.A. and Storey, B.T. (1986). Bicarbonate is essential for fertilization of mouse eggs: mouse sperm require it to undergo the acrosome reaction. Biol Reprod. 34(2): p. 349-56.
Neill, J.M. and Olds-Clarke, P. (1987). A computer-assisted assay for mouse sperm hyperactivation demonstrates that bicarbonate but not bovine serum albumin is required. Gamete Res. 18(2): p. 121-40.
Shi, Q.X. and Roldan, E.R. (1995). Bicarbonate/CO2 is not required for zona pellucida- or progesterone-induced acrosomal exocytosis of mouse spermatozoa but is essential for capacitation. Biol Reprod. 52(3): p. 540-6.
Parrish, J.J., Susko-Parrish, J.L., and First, N.L. (1989). Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biol Reprod. 41(4): p. 683-99.
Zeng, Y., Oberdorf, J.A., and Florman, H.M. (1996). pH regulation in mouse sperm: identification of Na(+)-, Cl(-)-, and HCO3(-)-dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev Biol. 173(2): p. 510-20.
Garbers, D.L., Tubb, D.J., and Hyne, R.V. (1982). A requirement of bicarbonate for Ca2+-induced elevations of cyclic AMP in guinea pig spermatozoa. J Biol Chem. 257(15): p. 8980-4.
Harrison, R.A. and Miller, N.G. (2000). cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Mol Reprod Dev. 55(2): p. 220-8.
Harrison, R.A. (2004). Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol Reprod Dev. 67(3): p. 337-52.
Hanoune, J. and Defer, N. (2001). Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol. 41: p. 145-74.
Conti, M., Andersen, C.B., Richard, F., Mehats, C., Chun, S.Y., Horner, K., Jin, C., and Tsafriri, A. (2002). Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol. 187(1-2): p. 153-9.
Pomorski, T., Herrmann, A., Zimmermann, B., Zachowski, A., and Müller, P. (1995). An improved assay for measuring the transverse redistribution of fluorescent phospholipids in plasma membranes. Chemistry and Physics of Lipids. 77(2): p. 139-146.
Nolan, J.P., Magargee, S.F., Posner, R.G., and Hammerstedt, R.H. (1995). Flow cytometric analysis of transmembrane phospholipid movement in bull sperm. Biochemistry. 34(12): p. 3907-15.
Salicioni, A.M., Platt, M.D., Wertheimer, E.V., Arcelay, E., Allaire, A., Sosnik, J., and Visconti, P.E. (2007). Signalling pathways involved in sperm capacitation. Soc Reprod Fertil Suppl. 65: p. 245-59.
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Battistone, M.A., Da Ros, V.G., Salicioni, A.M., Navarrete, F.A., Krapf, D., Visconti, P.E., and Cuasnicú, P.S. (2013). Functional human sperm capacitation requires both bicarbonate-dependent PKA activation and down-regulation of Ser/Thr phosphatases by Src family kinases. Mol Hum Reprod. 19(9): p. 570-80.
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Wasco, W.M. and Orr, G.A. (1984). Function of calmodulin in mammalian sperm: presence of a calmodulin-dependent cyclic nucleotide phosphodiesterase associated with demembranated rat caudal epididymal sperm. Biochem Biophys Res Commun. 118(2): p. 636-42.
Leclerc, P., de Lamirande, E., and Gagnon, C. (1998). Interaction between Ca2+, cyclic 3',5' adenosine monophosphate, the superoxide anion, and tyrosine phosphorylation pathways in the regulation of human sperm capacitation. J Androl. 19(4): p. 434-43.
Carrera, A., Moos, J., Ning, X.P., Gerton, G.L., Tesarik, J., Kopf, G.S., and Moss, S.B. (1996). Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation. Dev Biol. 180(1): p. 284-96.
Tateno, H., Krapf, D., Hino, T., Sánchez-Cárdenas, C., Darszon, A., Yanagimachi, R., and Visconti, P.E. (2013). Ca2+ ionophore A23187 can make mouse spermatozoa capable of fertilizing in vitro without activation of cAMP-dependent phosphorylation pathways. Proceedings of the National Academy of Sciences. 110(46): p. 18543-18548.
Referanslar
Barratt, C.L., Kay, V., and Oxenham, S.K. (2009). The human spermatozoon - a stripped down but refined machine. J Biol. 8(7): p. 63.
Brewer, L., Corzett, M., and Balhorn, R. (2002). Condensation of DNA by Spermatid Basic Nuclear Proteins*. Journal of Biological Chemistry. 277(41): p. 38895-38900.
Dadoune, J.P. (2003). Expression of mammalian spermatozoal nucleoproteins. Microsc Res Tech. 61(1): p. 56-75.
Fauci, L.J. and Dillon, R. (2006). BIOFLUIDMECHANICS OF REPRODUCTION. Annual Review of Fluid Mechanics. 38(Volume 38, 2006): p. 371-394.
Oko, R.J. (1995). Developmental expression and possible role of perinuclear theca proteins in mammalian spermatozoa. Reprod Fertil Dev. 7(4): p. 777-97.
Bozkurt, H.H. and Woolley, D.M. (1993). Morphology of nexin links in relation to interdoublet sliding in the sperm flagellum. Cell Motil Cytoskeleton. 24(2): p. 109-18.
Brokaw, C.J. (2009). Thinking about flagellar oscillation. Cell Motility. 66(8): p. 425-436.
DiBella, L.M. and King, S.M. (2001). Dynein motors of the Chlamydomonas flagellum. Int Rev Cytol. 210: p. 227-68.
Porter, M.E. and Sale, W.S. (2000). The 9 + 2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J Cell Biol. 151(5): p. F37-42.
Takada, S., Wilkerson, C.G., Wakabayashi, K., Kamiya, R., and Witman, G.B. (2002). The outer dynein arm-docking complex: composition and characterization of a subunit (oda1) necessary for outer arm assembly. Mol Biol Cell. 13(3): p. 1015-29.
Brokaw, C.J. and Kamiya, R. (1987). Bending patterns of Chlamydomonas flagella: IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function. Cell Motility. 8(1): p. 68-75.
Brokaw, C.J., Josslin, R., and Bobrow, L. (1974). Calcium ion regulation of flagellar beat symmetry in reactivated sea urchin spermatozoa. Biochem Biophys Res Commun. 58(3): p. 795-800.
Inaba, K. (2002). Dephosphorylation of Tctex2-related dynein light chain by type 2A protein phosphatase. Biochem Biophys Res Commun. 297(4): p. 800-5.
Gagnon, C., White, D., Cosson, J., Huitorel, P., Eddé, B., Desbruyères, E., Paturle-Lafanechère, L., Multigner, L., Job, D., and Cibert, C. (1996). The polyglutamylated lateral chain of alpha-tubulin plays a key role in flagellar motility. J Cell Sci. 109 ( Pt 6): p. 1545-53.
Huitorel, P., White, D., Fouquet, J.P., Kann, M.L., Cosson, J., and Gagnon, C. (2002). Differential distribution of glutamylated tubulin isoforms along the sea urchin sperm axoneme. Mol Reprod Dev. 62(1): p. 139-48.
Lindemann, C.B. and Lesich, K.A. (2010). Flagellar and ciliary beating: the proven and the possible. J Cell Sci. 123(Pt 4): p. 519-28.
O'Rand, M.G. and Widgren, E.E. (2012). Loss of calcium in human spermatozoa via EPPIN, the semenogelin receptor. Biol Reprod. 86(2): p. 55.
Wennemuth, G., Babcock, D.F., and Hille, B. (2003). Calcium clearance mechanisms of mouse sperm. J Gen Physiol. 122(1): p. 115-28.
Harper, C., Wootton, L., Michelangeli, F., Lefièvre, L., Barratt, C., and Publicover, S. (2005). Secretory pathway Ca2+-ATPase (SPCA1) Ca2+ pumps, not SERCAs, regulate complex [Ca2+]i signals in human spermatozoa. Journal of Cell Science. 118(8): p. 1673-1685.
Chang, M.C. (1951). Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature. 168(4277): p. 697-8.
Austin, C.R. (1951). Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res B. 4(4): p. 581-96.
Aitken, R.J. and Nixon, B. (2013). Sperm capacitation: a distant landscape glimpsed but unexplored. Mol Hum Reprod. 19(12): p. 785-93.
Aitken, R.J., Harkiss, D., Knox, W., Paterson, M., and Irvine, D.S. (1998). A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation. J Cell Sci. 111 ( Pt 5): p. 645-56.
Aitken, R.J., Harkiss, D., Knox, W., Paterson, M., and Irvine, S. (1998). On the cellular mechanisms by which the bicarbonate ion mediates the extragenomic action of progesterone on human spermatozoa. Biol Reprod. 58(1): p. 186-96.
Baker, M.A., Hetherington, L., and Aitken, R.J. (2006). Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa. J Cell Sci. 119(Pt 15): p. 3182-92.
Ecroyd, H., Asquith, K.L., Jones, R.C., and Aitken, R.J. (2004). The development of signal transduction pathways during epididymal maturation is calcium dependent. Dev Biol. 268(1): p. 53-63.
Visconti, P.E., Bailey, J.L., Moore, G.D., Pan, D., Olds-Clarke, P., and Kopf, G.S. (1995). Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development. 121(4): p. 1129-37.
Devi, K.U., Jha, K., and Shivaji, S. (1999). Plasma membrane-associated protein tyrosine phosphatase activity in hamster spermatozoa. Mol Reprod Dev. 53(1): p. 42-50.
Galantino-Homer, H.L., Visconti, P.E., and Kopf, G.S. (1997). Regulation of Protein Tyrosine Phosphorylation during Bovine Sperm Capacitation by a Cyclic Adenosine 3',5'-Monophosphate-Dependent Pathway1. Biology of Reproduction. 56(3): p. 707-719.
Kalab, P., Peknicová, J., Geussová, G., and Moos, J. (1998). Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway. Mol Reprod Dev. 51(3): p. 304-14.
Luconi, M., Krausz, C., Forti, G., and Baldi, E. (1996). Extracellular calcium negatively modulates tyrosine phosphorylation and tyrosine kinase activity during capacitation of human spermatozoa. Biol Reprod. 55(1): p. 207-16.
Demarco, I.A., Espinosa, F., Edwards, J., Sosnik, J., De La Vega-Beltran, J.L., Hockensmith, J.W., Kopf, G.S., Darszon, A., and Visconti, P.E. (2003). Involvement of a Na+/HCO-3 cotransporter in mouse sperm capacitation. J Biol Chem. 278(9): p. 7001-9.
Chen, Y., Cann, M.J., Litvin, T.N., Iourgenko, V., Sinclair, M.L., Levin, L.R., and Buck, J. (2000). Soluble Adenylyl Cyclase as an Evolutionarily Conserved Bicarbonate Sensor. Science. 289(5479): p. 625-628.
Harrison, R.A., Ashworth, P.J., and Miller, N.G. (1996). Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev. 45(3): p. 378-91.
Gadella, B.M. and Harrison, R.A. (2002). Capacitation induces cyclic adenosine 3',5'-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod. 67(1): p. 340-50.
Flesch, F.M., Brouwers, J.F., Nievelstein, P.F., Verkleij, A.J., van Golde, L.M., Colenbrander, B., and Gadella, B.M. (2001). Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci. 114(Pt 19): p. 3543-55.
Boatman, D.E. and Robbins, R.S. (1991). Bicarbonate: carbon-dioxide regulation of sperm capacitation, hyperactivated motility, and acrosome reactions. Biol Reprod. 44(5): p. 806-13.
Gadella, B.M., Miller, N.G., Colenbrander, B., van Golde, L.M., and Harrison, R.A. (1999). Flow cytometric detection of transbilayer movement of fluorescent phospholipid analogues across the boar sperm plasma membrane: elimination of labeling artifacts. Mol Reprod Dev. 53(1): p. 108-25.
Lee, M.A. and Storey, B.T. (1986). Bicarbonate is essential for fertilization of mouse eggs: mouse sperm require it to undergo the acrosome reaction. Biol Reprod. 34(2): p. 349-56.
Neill, J.M. and Olds-Clarke, P. (1987). A computer-assisted assay for mouse sperm hyperactivation demonstrates that bicarbonate but not bovine serum albumin is required. Gamete Res. 18(2): p. 121-40.
Shi, Q.X. and Roldan, E.R. (1995). Bicarbonate/CO2 is not required for zona pellucida- or progesterone-induced acrosomal exocytosis of mouse spermatozoa but is essential for capacitation. Biol Reprod. 52(3): p. 540-6.
Parrish, J.J., Susko-Parrish, J.L., and First, N.L. (1989). Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biol Reprod. 41(4): p. 683-99.
Zeng, Y., Oberdorf, J.A., and Florman, H.M. (1996). pH regulation in mouse sperm: identification of Na(+)-, Cl(-)-, and HCO3(-)-dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev Biol. 173(2): p. 510-20.
Garbers, D.L., Tubb, D.J., and Hyne, R.V. (1982). A requirement of bicarbonate for Ca2+-induced elevations of cyclic AMP in guinea pig spermatozoa. J Biol Chem. 257(15): p. 8980-4.
Harrison, R.A. and Miller, N.G. (2000). cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Mol Reprod Dev. 55(2): p. 220-8.
Harrison, R.A. (2004). Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol Reprod Dev. 67(3): p. 337-52.
Hanoune, J. and Defer, N. (2001). Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol. 41: p. 145-74.
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